Individual variation and hormonal modulation of sodium channel alpha and beta1 subunits int he electric organ correlate with variation in a social signal

by 1976- Liu, He

Abstract (Summary)

The electric fish Sternopygus macrurus emits an electric organ discharge
(EOD) composed of a series of pulses. EOD frequency and duration are
individually unique, sexually dimorphic and regulated by steroid hormones.
Previous studies have shown the EOD pulse is partially shaped by a sodium
current, whose rate and voltage dependence of inactivation correlate with EOD
frequency and pulse duration, and are modulated by androgens.
In this study I tested whether the gradient in sodium current inactivation
across EOD frequency might be due to regulation on sodium channel ? and ?1
subunits. Full-length sequences of the two sodium channel ? subunits in the
electric organ of Sternopygus macrurus, smNav1.4a and smNav1.4b were
cloned. Furthermore, two smNav1.4b mRNA transcripts (smNav1.4bL and
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smNav1.4bS), with alternative first exons and translated into proteins with and
without an extended N terminus respectively, were identified. Electric organ
expresses smNav1.4a and smNav1.4b at comparable levels and preferentially
expresses smNav1.4bL. The mRNA level of smNav1.4bL but not smNav1.4a,
correlates with EOD frequency.
I also cloned the sodium channel ?1 subunit in Sternopygus and found two
splice forms of this gene (?1L and ?1S). They exhibit a distinct pattern of
differential expression in different tissues. In the electric organ, the mRNA levels
of ?1 and the splicing preference for ?1S correlate with EOD frequency.
An androgen implant lowered EOD frequency. It also lowered the mRNA
levels of smNav1.4bL, smNav1.4bS and ?1, but did not affect smNav1.4a or the
splicing preference of ?1.
Expression of smNav1.4bL or smNav1.4bS alone, or together with ?1L or
?1S in Xenopus oocytes revealed the kinetic properties of these subunits.
Importantly, smNav1.4bL and ?1S, whose expressions correlate with EOD
frequency, show faster inactivation rates and negative shifts of voltage
dependence, consistent with the natural phenotype of high EOD frequency fish.
Furthermore, two mutagenesis studies addressed the functions of the novel
regions in smNav1.4bL and ?1S.
These results suggest multiple levels of mRNA control on sodium channel
? and ?1 subunits underlie the cellular excitability in the electric organ and
correlate with the variation in an important social signal, EOD, in Sternopygus.
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